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SARS-Cov-2 Spike Opening Dynamics and Energetics Reveal the Individual Roles of Glycans and Their Collective Impact

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SARS-Cov-2 Spike Opening Dynamics and Energetics Reveal the Individual Roles of Glycans and Their Collective Impact bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. SARS-CoV-2 spike opening dynamics and energetics reveal the individual roles of glycans and their collective impact Yui Tik Pang,y,z Atanu Acharya,y,z Diane L. Lynch,y Anna Pavlova,y and James C. Gumbart∗,y ySchool of Physics, Georgia Institute of Technology, Atlanta, GA 30332 zContributed equally to this work E-mail: [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Abstract The trimeric spike (S) glycoprotein, which protrudes from the SARS-CoV-2 viral envelope, is responsible for binding to human ACE2 receptors. The binding process is initiated when the receptor binding domain (RBD) of at least one protomer switches from a “down” (closed) to an “up” (open) state. Here, we used molecular dynamics simulations and two-dimensional replica exchange umbrella sampling calculations to investigate the transition between the two S-protein conformations with and without glycosylation. We show that the glycosylated spike has a higher barrier to opening than the non-glycosylated one with comparable populations of the down and up states. In contrast, we observed that the up conformation is favored without glycans. Analysis of the S-protein opening pathway reveals that glycans at N165 and N122 interfere with hydrogen bonds between the RBD and the N-terminal domain in the up state. We also identify roles for glycans at N165 and N343 in stabilizing the down and up states. Finally we estimate how epitope exposure for several known antibodies changes along the opening path. We find that the epitope of the BD-368-2 antibody remains exposed irrespective of the S-protein conformation, explaining the high efficacy of this antibody. 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Introduction The ongoing COVID-19 pandemic caused by the SARS-CoV-2 coronavirus quickly spread worldwide with unprecedented detrimental impact on global health and economies.1 Al- though deployment is ongoing and not uniform worldwide, the rapid development of several vaccines2 as well as monoclonal antibody treatments3 have produced the first successful phase in mitigating the current viral outbreak. However, the emerging threat of variants4,5 and the possibility of future coronavirus outbreaks6 necessitate a thorough understanding of the viral life cycle, including recognition, binding, and infection. SARS-CoV-2 infection is initiated by the recognition of, and binding to, the host-cell angiotensin-converting enzyme 2 (ACE2) receptor.7,8 This process is mediated by the SARS- CoV-2 spike (S) protein, a homotrimeric class I fusion glycoprotein that protrudes from the surface of the SARS-CoV-2 virion. Release of the S-protein sequence in early 2020, combined with earlier structural work on related betacoronaviruses, has led to the rapid determination of structures of solublized, pre-fusion stablized S-protein ectodomain constructs9–14 (Fig. 1). Each protomer consists of the S1 and S2 subunits separated by a multibasic furin cleav- age site. S1 contains the receptor binding domain (RBD) and mediates host cell recognition while S2 consists of the membrane fusion machinery necessary for viral entry.7 The S-protein is a major antigenic target with multiple epitopes that are targeted by the human immune system, including the RBD and the N-terminal domain (NTD).5,15–17 Moreover, glycosy- lation of the S-protein aids in masking and shielding the virus from host immune system response.18–20 The S-protein is characterized by down and up conformational states, which transiently interconvert via a hinge-like motion exposing the receptor binding motif (RBM), which is composed of RBD residues S438 to Q506.21 The RBM is buried in the inter-protomer interface of the down S-protein; therefore, binding to ACE2 relies on the stochastic inter- conversion between the down and up states. Cryo-electron microscopy (cryo-EM) studies have revealed detailed structural informa- tion for both the up and down conformational states.22 However, relatively few studies have 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Figure 1: S-protein of SARS-CoV-2. (a) The trimeric S-protein in the all-down state, colored by protomer. Glycans are shown as red spheres. (b) Top view of the S-protein in the one-up state. Important domains of the spike are highlighted, including the N-terminal domain (NTD, 14–306), the receptor binding domains (RBD, 336–518), the heptad repeat 1 (HR1, 908–986), and the central helix (CH, 987–1035). (c,d) The two collective variables defined to describe the opening of RBD-A include: (c) the center-of-mass distance d between RBD- A (pink) and SD1-B (lime), and (d) the dihedral angle ϕ formed by the domains RBD-A (pink), SD1-A (purple), SD2-A (ice blue), and NTD-A (cyan). RBD-A in both the down (solid pink) and up (transparent pink) states are shown. explored the dynamics of these up/down states and interconversion between them. For ex- ample, single-molecule FRET has been used to demonstrate the stochastic nature of the S-protein transitions,23 with reported timescales on the order of milliseconds to seconds. Molecular dynamics (MD) simulations complement these experimental studies by providing the atomic-level descriptions of intermediate states between down and up that are necessary to characterize S-protein opening dynamics. MD simulations have revealed detailed infor- mation about the structural stability and the role of glycosylation for both the down and up states, as well as for inter-residue interactions and details of binding to ACE2.19,20,24–26 Opening pathways determined using steered MD and targeted MD have been reported.26–28 More recently, extensive simulations using enhanced sampling techniques such as weighted ensemble29 and fluctuation amplification of specific traits (FAST) adaptive sampling com- bined with Folding@home30 have provided details of multiple pathways for the S-protein opening. Moreover, features of the energy landscape of these conformational transitions 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. that are necessary for viral binding and entry are beginning to emerge.27,28,31 A recent study by Amaro and coworkers has highlighted the functional role of glycans at N165 and N234 beyond shielding24 based on separate equilibrium simulations of the S- protein down and up states. When the RBD transitions to the up state, the glycan at N234 rotates into the resulting void, stablizing the up conformation. Moreover, MD simulations and mutagenesis have revealed contributions of the glycan at N343 to the dynamics of RBD opening and ACE2 binding.29 These results suggested a role for the glycan at N343 in the opening conformational transition via “lifting” the RBD through sequential interactions with multiple RBD residues, referred to as “glycan gating”. Here, we describe newly determined two-dimensional (2D) free-energy landscapes of the SARS-CoV-2 S-protein opening and closing transitions using replica exchange umbrella sam- pling (REUS) simulations for glycosylated as well as un-glycosylated S-protein. We highlight the impact of glycans on each state and on the kinetics of spike opening. Furthermore, we analyzed the exposure of prominent epitopes on the S-protein surface and provide a dynamic picture of antibody binding along the spike-opening path. Finally we report the results of equilibrium MD simulations of the glycosylated and un-glycosylated systems for the down as well as up conformational states in order to further characterize the stabilizing role of the glycans. Results Glycans modulate the energetics and pathway of spike opening Using REUS simulations, we studied the free-energy change from the down state of spike to the up state when fully glycoslyated as well as when un-glycosylated. We modeled the wild-type (WT) up state based on the diproline mutant structure from Walls et al.10 (PDB: 6VYB). The down-state was modeled using a more recent structure from Cai et al.11 (PDB: 6XR8) without the diproline mutations. The glycan with highest population in the mass 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.12.456168; this version posted August 13, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. spectroscopy data from Crispin and coworkers18 at each site was added using the GLYCAM Web server developed by the Woods group (http://glycam.org).32,33 Additional details of the system are provided in Methods. We first ran metadynamics simulations of the cryo-EM structures in the down andup states, allowing them to explore the conformational space between them. This space is described by two collective variables, which are (1) the center-of-mass distance (d) between the opening RBD-A and a stationary part of the spike acting as a pivot point, namely the neighboring subdomain 2 on chain B (SD2-B), and (2) the dihedral angle (ϕ) formed by the opening RBD-A and other stationary domains on the same protomer, namely SD2-A, SD1-A and NTD-A (Fig.
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